 |
||||
|
||||
|
||||
|
||||
Previous Article | Next Article
The Journal of Neuroscience, June 15, 2001, 21(12):4195-4206
Synapsin Controls Both Reserve and Releasable Synaptic Vesicle Pools during Neuronal Activity and Short-Term Plasticity in Aplysia
Yann Humeau1, Frédéric Doussau1, Francesco Vitiello1, Paul Greengard2, Fabio Benfenati2, 3, and Bernard Poulain1 1 Neurotransmission et Sécrétion Neuroendocrine, Centre National de la Recherche Scientifique, IFR-37 des Neurosciences, F-67084 Strasbourg Cédex, France, 2 Laboratory of Molecular and Cellular Neuroscience, The Rockefeller University, New York, New York 10021-6399, and 3 Department of Experimental Medicine, Section of Human Physiology, University of Genova, 16132 Genova, Italy
Neurotransmitter release is a highly efficient secretory process exhibiting resistance to fatigue and plasticity attributable to the existence of distinct pools of synaptic vesicles (SVs), namely a readily releasable pool and a reserve pool from which vesicles can be recruited after activity. Synaptic vesicles in the reserve pool are thought to be reversibly tethered to the actin-based cytoskeleton by the synapsins, a family of synaptic vesicle-associated phosphoproteins that have been shown to play a role in the formation, maintenance, and regulation of the reserve pool of synaptic vesicles and to operate during the post-docking step of the release process. In this paper, we have investigated the physiological effects of manipulating synapsin levels in identified cholinergic synapses of Aplysia californica. When endogenous synapsin was neutralized by the injection of specific anti-synapsin antibodies, the amount of neurotransmitter released per impulse was unaffected, but marked changes in the secretory response to high-frequency stimulation were observed, including the disappearance of post-tetanic potentiation (PTP) that was substituted by post-tetanic depression (PTD), and increased rate and extent of synaptic depression. Opposite changes on post-tetanic potentiation were observed when synapsin levels were increased by injecting exogenous synapsin I. Our data demonstrate that the presence of synapsin-dependent reserve vesicles allows the nerve terminal to release neurotransmitter at rates exceeding the synaptic vesicle recycling capacity and to dynamically change the efficiency of release in response to conditioning stimuli (e.g., post-tetanic potentiation). Moreover, synapsin-dependent regulation of the fusion competence of synaptic vesicles appears to be crucial for sustaining neurotransmitter release during short periods at rates faster than the replenishment kinetics and maintaining synchronization of quanta in evoked release.
Key words: Aplysia; synapse; exocytosis; neurotransmitter release; short-term plasticity; synaptic depression; post-tetanic potentiation
Copyright © 2001 Society for Neuroscience 0270-6474/01/21124195-12$05.00/0
This article has been cited by other articles:
W. L. Coleman, C. A. Bill, F. Simsek-Duran, G. Lonart, D. Samigullin, and M. Bykhovskaia
Synapsin II and calcium regulate vesicle docking and the cross-talk between vesicle pools at the mouse motor terminals
J. Physiol., October 1, 2008; 586(19): 4649 - 4673.
[Abstract] [Full Text] [PDF]
A. Corradi, A. Zanardi, C. Giacomini, F. Onofri, F. Valtorta, M. Zoli, and F. Benfenati
Synapsin-I- and synapsin-II-null mice display an increased age-dependent cognitive impairment
J. Cell Sci., September 15, 2008; 121(18): 3042 - 3051.
[Abstract] [Full Text] [PDF]
P. Baldelli, A. Fassio, F. Valtorta, and F. Benfenati
Lack of Synapsin I Reduces the Readily Releasable Pool of Synaptic Vesicles at Central Inhibitory Synapses
J. Neurosci., December 5, 2007; 27(49): 13520 - 13531.
[Abstract] [Full Text] [PDF]
D. Fioravante, R.-Y. Liu, A. K. Netek, L. J. Cleary, and J. H. Byrne
Synapsin Regulates Basal Synaptic Strength, Synaptic Depression, and Serotonin-Induced Facilitation of Sensorimotor Synapses in Aplysia
J Neurophysiol, December 1, 2007; 98(6): 3568 - 3580.
[Abstract] [Full Text] [PDF]
F. Fiumara, C. Milanese, A. Corradi, S. Giovedi, G. Leitinger, A. Menegon, P. G. Montarolo, F. Benfenati, and M. Ghirardi
Phosphorylation of synapsin domain A is required for post-tetanic potentiation
J. Cell Sci., September 15, 2007; 120(18): 3228 - 3237.
[Abstract] [Full Text] [PDF]
Y. Humeau, F. Doussau, M. R. Popoff, F. Benfenati, and B. Poulain
Fast changes in the functional status of release sites during short-term plasticity: involvement of a frequency-dependent bypass of Rac at Aplysia synapses
J. Physiol., September 15, 2007; 583(3): 983 - 1004.
[Abstract] [Full Text] [PDF]
A. Alaedini, H. Okamoto, C. Briani, K. Wollenberg, H. A. Shill, K. O. Bushara, H. W. Sander, P. H. R. Green, M. Hallett, and N. Latov
Immune Cross-Reactivity in Celiac Disease: Anti-Gliadin Antibodies Bind to Neuronal Synapsin I
J. Immunol., May 15, 2007; 178(10): 6590 - 6595.
[Abstract] [Full Text] [PDF]
A. Fassio, D. Merlo, J. Mapelli, A. Menegon, A. Corradi, M. Mete, S. Zappettini, G. Bonanno, F. Valtorta, E. D'Angelo, et al.
The synapsin domain E accelerates the exoendocytotic cycle of synaptic vesicles in cerebellar Purkinje cells
J. Cell Sci., October 15, 2006; 119(20): 4257 - 4268.
[Abstract] [Full Text] [PDF]
A. Kielland, A. Erisir, S. I. Walaas, and P. Heggelund
Synapsin Utilization Differs among Functional Classes of Synapses on Thalamocortical Cells
J. Neurosci., May 24, 2006; 26(21): 5786 - 5793.
[Abstract] [Full Text] [PDF]
J. Sun, P. Bronk, X. Liu, W. Han, and T. C. Sudhof
Synapsins regulate use-dependent synaptic plasticity in the calyx of Held by a Ca2+/calmodulin-dependent pathway
PNAS, February 21, 2006; 103(8): 2880 - 2885.
[Abstract] [Full Text] [PDF]
O. Hvalby, V. Jensen, H.-T. Kao, and S. I. Walaas
Synapsin-regulated synaptic transmission from readily releasable synaptic vesicles in excitatory hippocampal synapses in mice
J. Physiol., February 15, 2006; 571(1): 75 - 82.
[Abstract] [Full Text] [PDF]
S. A. Kushner, Y. Elgersma, G. G. Murphy, D. Jaarsma, G. M. van Woerden, M. R. Hojjati, Y. Cui, J. C. LeBoutillier, D. F. Marrone, E. S. Choi, et al.
Modulation of Presynaptic Plasticity and Learning by the H-ras/Extracellular Signal-Regulated Kinase/Synapsin I Signaling Pathway
J. Neurosci., October 19, 2005; 25(42): 9721 - 9734.
[Abstract] [Full Text] [PDF]
S. Hilfiker, F. Benfenati, F. Doussau, A. C. Nairn, A. J. Czernik, G. J. Augustine, and P. Greengard
Structural Domains Involved in the Regulation of Transmitter Release by Synapsins
J. Neurosci., March 9, 2005; 25(10): 2658 - 2669.
[Abstract] [Full Text] [PDF]
T. Galli and V. Haucke
Cycling of Synaptic Vesicles: How Far? How Fast!
Sci. Signal., December 21, 2004; 2004(264): re19 - re19.
[Abstract] [Full Text] [PDF]
D. Gitler, Y. Takagishi, J. Feng, Y. Ren, R. M. Rodriguiz, W. C. Wetsel, P. Greengard, and G. J. Augustine
Different Presynaptic Roles of Synapsins at Excitatory and Inhibitory Synapses
J. Neurosci., December 15, 2004; 24(50): 11368 - 11380.
[Abstract] [Full Text] [PDF]
S. Giovedi, P. Vaccaro, F. Valtorta, F. Darchen, P. Greengard, G. Cesareni, and F. Benfenati
Synapsin Is a Novel Rab3 Effector Protein on Small Synaptic Vesicles: I. IDENTIFICATION AND CHARACTERIZATION OF THE SYNAPSIN I-Rab3 INTERACTIONS IN VITRO AND IN INTACT NERVE TERMINALS
J. Biol. Chem., October 15, 2004; 279(42): 43760 - 43768.
[Abstract] [Full Text] [PDF]
S. Giovedi, F. Darchen, F. Valtorta, P. Greengard, and F. Benfenati
Synapsin Is a Novel Rab3 Effector Protein on Small Synaptic Vesicles: II. FUNCTIONAL EFFECTS OF THE Rab3A-SYNAPSIN I INTERACTION
J. Biol. Chem., October 15, 2004; 279(42): 43769 - 43779.
[Abstract] [Full Text] [PDF]
F. Fiumara, S. Giovedi, A. Menegon, C. Milanese, D. Merlo, P. G. Montarolo, F. Valtorta, F. Benfenati, and M. Ghirardi
Phosphorylation by cAMP-dependent protein kinase is essential for synapsin-induced enhancement of neurotransmitter release in invertebrate neurons
J. Cell Sci., October 1, 2004; 117(21): 5145 - 5154.
[Abstract] [Full Text] [PDF]
J. Schmoranzer and S. M. Simon
Role of Microtubules in Fusion of Post-Golgi Vesicles to the Plasma Membrane
Mol. Biol. Cell, April 1, 2003; 14(4): 1558 - 1569.
[Abstract] [Full Text] [PDF]
M. M. Rich, X. Wang, T. C. Cope, and M. J. Pinter
Reduced Neuromuscular Quantal Content With Normal Synaptic Release Time Course and Depression in Canine Motor Neuron Disease
J Neurophysiol, December 1, 2002; 88(6): 3305 - 3314.
[Abstract] [Full Text] [PDF]
Y. Humeau, M. R. Popoff, H. Kojima, F. Doussau, and B. Poulain
Rac GTPase Plays an Essential Role in Exocytosis by Controlling the Fusion Competence of Release Sites
J. Neurosci., September 15, 2002; 22(18): 7968 - 7981.
[Abstract] [Full Text] [PDF]
A. Angers, D. Fioravante, J. Chin, L. J. Cleary, A. J. Bean, and J. H. Byrne
Serotonin Stimulates Phosphorylation of Aplysia Synapsin and Alters Its Subcellular Distribution in Sensory Neurons
J. Neurosci., July 1, 2002; 22(13): 5412 - 5422.
[Abstract] [Full Text] [PDF]
Y. Humeau, N. Vitale, S. Chasserot-Golaz, J.-L. Dupont, G. Du, M. A. Frohman, M.-F. Bader, and B. Poulain
A role for phospholipase D1 in neurotransmitter release
PNAS, December 18, 2001; 98(26): 15300 - 15305.
[Abstract] [Full Text] [PDF]
|
|
|
|
 |
|